ARTIGO_First record of a phoretic mite (Histiostomatidae) on a cave dwelling cricket (Phalangopsidae) from Brazil

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Abstract

The first record of a phoretic mite of the genus Histiostoma (Sarcoptiformes: Histiostoma-tidae) associated with an individual of Endecous (Endecous) alejomesai (Orthoptera: Pha-langopsidae) is reported from a Brazilian cave. Although deutonymphs of histiostomatid mites are common phoretic on invertebrates, this is the first report of their phoretic associ-ation with a cave dwelling cricket.

Keywords: Histiostoma, Endecous, simbiosis, hypogean habitat.

Resumo

O primeiro registro do ácaro forético do gênero Histiostoma (Sarcoptiformes: Histiostoma-tidae) associado a um indivíduo de Endecous (Endecous) alejomesai (Orthoptera: Pha-langopsidae) é relatado para uma caverna brasileira. Embora as deutoninfas de ácaros sejam comumente encontradas realizando forese em invertebrados, esse é o primeiro relato de sua associação com um grilo cavernícola.

Palavras-chave: Histiostoma, Endecous, simbiose, habitat hipógeo. SHORT COMMUNICATION

First record of a phoretic mite (Histiostomatidae) on a cave

dwelling cricket (Phalangopsidae) from Brazil

Primeiro registro de ácaros foréticos (Histiostomatidae) em um grilo

cavernícola (Phalangopsidae) no Brasil

1_{Universidade Federal de Lavras. Departamento de}

Bio-logia. Programa de Pós-Graduação em Ecologia Aplicada. Caixa Postal 3037, Campus Universitário, 37200-000, Lavras, MG, Brasil.

Biologia. Centro de Estudos em Biologia Subterrânea. Caixa postal 3037, Campus Universitário, 37200-000, Lavras, MG, Brasil.

Biologia. Setor de Ecologia. Programa Nacional de Pós--Doutorado (PNPD/CAPES). Caixa postal 3037, Campus Universitário, 37200-000, Lavras, MG, Brasil.

Rodrigo Antônio Castro Souza1,2

rodrigodesouzaac@gmail.com

Leopoldo Ferreira de Oliveira Bernardi3

leopoldobernardi@gmail.com

Rodrigo Lopes Ferreira²

drops@dbi.ufla.br

Phoresis is a common type of symbiosis between live animals represent-ing an interspecific association in which one organism (phoretic) attaches for an unlimited period of time to another (host) strictly with the aim to disperse (Houck and OConnor, 1991; Knülle, 2003; Reynolds et al., 2014). Such type of interaction is common in habitats where the conditions rapidly changes and/or when the resources are ephemeral (e.g. feces and carcasses) (Farish and Axtell, 1971; Houck and OConnor, 1991). Cave organisms are frequently supported by ephemeral resources from the surface imported by biotic (e.g. bats) or abi-otic agents (e.g. water courses, wind). In general, these agents are inefficient in this transport, what results in the oligotrophic condition commonly observed in caves (Culver and Pipan, 2009).

Mites of the family Histiostomatidae, such as the species of the genus

His-tiostoma (Acariformes, Astigmatina, HisHis-tiostomatoidea) are among the species

that use such phoretic strategy of dispersion and represent one of the largest groups within Astigmatina, with more than 500 described species (Schatz et al., 2011). These species are found living free in the soil and in decomposing

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or-ganic matter both in epigean and hypogean environments, generally during the deutonymph phase (hypopus stage), and also may be found phoreticaly associated to other in-vertebrates (Houck and OConnor, 1991). The exceptions to this lifestyle are a few described species, parasites of fish, leeches, and worm eggs (Fain and Lambrechts 1987; Halliday and Collins 2002; Hughes and Jackson, 1958).

During their life cycle, the Histiostomatidae mites, such as other Astigmatina groups, may turn into hypopus which are deutonymphs specialized on dispersing (Houck and OConnor, 1991; OConnor, 1994). In most species, the hypopus shows morphological adaptations, such as an anal sucker plate, by means of which the mite fastens in its vector (Houck and OConnor, 1991; OConnor, 1994). Although the hypopus usually do not feed, some species may take advantage of the close corporal relationship with the host, parasitizing it, andabsorbing compounds in form of a fluid, such as water (Houck and Cohen, 1995). This phase usually occurs in a given population when the mites are in environmentally unsuitable locations, or when the population grows very sharply. In these cases, individu-als migrate for other habitats associated with their hosts, since the mites have little ability to move (Farish and Ax-tell, 1971).

Histiostomatidae are known by using a great diversity of arthopods as hosts in the epigean environment, such as arachnids (Dunlop et al., 2012; Fain, 1991; Vachon, 1940), centipedes (Fain, 1991), coleopterans (Fain and Santiago-Blay, 1993; Wirth et al., 2016; Wirth and Pernek, 2012), dipterans, earwigs, cockroaches (Negm and Alatawi, 2011; Pimsler et al., 2016; Tagami, 2013; Chmielewski, 2009), hymenopterans (Fain and Erteld, 1998; Fain and Pauly, 2001; Uppstrom and Klompen, 2011), springtails (Fain and Johnston, 1974), among others arthropods. However, few cases of Histiostomatidae using orthopterans as dis-perser hosts are recorded: a single association with crickets (Gryllidae: Gryllus bimaculatus) in Saudi Arabia (Negm and Alatawi, 2011) and other with sandgropers (Cylin-drachetidae: Cylindraustralia kochii and C. tindalei) in Australia (Houston, 2007). On the other hand, despite that occurrences of Histiostomatidae in the cave environment are common (Bernardi et al., 2009; Cokendolpher and Pol-yak, 1996; Palacios-Vargas et al., 2011; Welbourn, 1999), mainly associated to bat guano (Ferreira et al., 2000; Pel-legrini and Ferreira, 2013), cases of phoresis involving this group have not been recorded. Therefore, the present work reports the first occurrence of histiostomaid mites at hy-popus stage associated to genus Endecous in a Brazilian cave, a commonly crickets found in subterranean cavities from South America (Cigliano et al., 2017).

The association reported in this study was observed during collections performed in Cabeceira D’Água cave (13°52’53.56’’S 46°55’44.31’’W), municipality of Nova Roma, Goiás, Brazil (Figure 1), on August 8, 2015. This

cave presents considerable dimensions, exceeding 4.5 Km of extension, and a stream runs in the main gallery of the cave. Along this main gallery there were discrete piles of guano and vegetal organic matter imported by the stream. Such organic substrates represent ideal places for repro-duction and foraging of mites and crickets, among other invertebrates (Ferreira et al., 2000; Pellegrini and Ferreira, 2013; Schneider et al., 2011).

During the expedition, sampling was carried out using the active search method, where all the potential biotopes that could possibly be used as food and shelter resource for fauna were examined (e.g. soil, remnants of matter or-ganic, under stones). All specimens collected were stored in individual vials containing 70% ethanol. The identifi-cation of the crickets was done by analyzing the external morphology and genital sclerites (from both males and females) using a stereomicroscope STEMI 2000 (Zeiss). The identification was based on taxonomic keys and spe-cies descriptions (Mello et al., 2013; Zefa et al., 2010). The photographs of the association between the crick-ets and mites were obtained using an Axion Zoom V16 (Zeiss) stereomicroscope. The identification of mites was given after the removal of individuals from the host, and mounting of specimens on glass slides, with the use of Hoyer’s medium. Specimens mounted on slides were kept in heather at 45ºC for 10 days. After that, each individual

Figure 1. Location of the cave Cabeceira d’Água, state of Goiás, Brazil, in South America.

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was identified through a morphological analysis using a microscope Axio Scope. A1 (Zeiss) equipped with Dif-ferential Interference Contrast (DIC) and with a coupled camera. Taxonomic keys used for identification are in the publications of Hughes and Jackson (1958), Walter et al. (2009), and Wirth (2004).

The mites were observed attached to the head of a sin-gle specimen of Endecous (Endecous) alejomesai Zefa 2010. The adult male cricket carried about 50 individuals of the genus Histiostoma (Sarcoptiformes: Histiostomati-dae), which were strongly adhered to all parts of the crick-et head, including the palp, basis of antenna, mandibular pieces and others (Figure 2). Both species were deposited in the Collection of Subterranean Invertebrates of Lavras (ISLA), Federal University of Lavras, Brazil. Unfortunate-ly, it was not possible to make progress in identifying the individuals of Histiostoma found in this study. In order to differentiate Histiostomatidae species or to describe a new species accurately, an analysis of both young and adult stages is necessary (Pernek et al., 2012; Wirth, 2004).

The association between histiosmatid mites and

Ende-cous is not common in the cave environment (and neither

was recorded for epigean habitats). Hundreds of individu-als from more than 236 caves from 13 Brazilian states has been analyzed in a taxonomic study on crickets of this

ge-nus from Brazilian caves (Castro-Souza, unpublished data) and the here reported association was observed only once. Histiostomatidae mites are frequently observed in Bra-zilian caves, which are mainly found in guano piles and de-composing organic matter (Bernardi et al., 2009; Ferreira and Martins, 2009; Pellegrini and Ferreira, 2013). Such or-ganic resources are commonly used by Endecous in their diet. Considering the fixation site of Histiostoma on the body of Endecous, as well as the habit of these two organ-isms, it is possible to infer that the mites probably migrated to the host while it was feeding. Given the great amount of individuals observed on the cricket head (Figure 3), the organic substrate was probably full of hypopus. Phoresy behavior presumably results in the dispersal of individuals from areas unsuited for further development, either of the individual or its progeny, to suitable environments (Farish and Axtell, 1971). In the case of some mites, such as the his-tiostomatid, the unfavorable environmental conditions (such as drying out, overcrowding, lack of food, and accumula-tion of waste products) favor the interposiaccumula-tion of the hypo-pus stage, which is adapted to dispersion by a host (Binns, 1982; Knülle, 2003; Reynolds et al., 2014). However, it is important to highlight that even considering caves as suit-able habitats for mites and crickets, it is possible that this is a sporadic and rare interaction given the number of crickets

Figure 2. Endecous (Endecous) alejomesai associated with numerous mites of the genus Histiostoma: cricket head in lateral (A), diago-nal (B), frontal (C) and dorsal (D) views. Red circles indicate histiostomatid mites attached to the head of the cricket.

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observed without mites during the studies regarding Brazil-ian cave fauna in the last years (Cajaiba, 2012; Souza-Dias

et al., 2014; Bolfarini and Bichuette, 2015; Castro-Souza et al., 2017; Cigliano et al., 2017).

The interaction between mites and their hosts is still poorly known regarding cave species. However, some as-sociations may constitute an interesting study object since caves are environments where the resources are in general scarce and ephemeral. Therefore, the phoretic dispersion may represent an essential habit for the survival and per-petuation of populations of organisms with reduced motil-ity, such as histiostomatid mites.

Acknowledgements

LFOB and RACS scholarships were provided by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior). Funding for the study was provided by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) and Conselho Nacional de Pesquisa to R.L.F. (CNPq grant nr. 304682/2014-4). Thanks to Pavel Klimov for helping in the mite identification. We are also grateful to Vanessa Mendes Martins, EGB (Espeleo Grupo de Brasília) and Edvard Magalhães for all support in the

field. We thank the editor and anonymous referees for helpful comments on the manuscript.

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Submitted on August 4, 2017 Accepted on March 29, 2018